Ancient DNA reveals selection acting on genes associated with hypoxia response in pre-Columbian Peruvian Highlanders in the last 8500 years

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Fehren Schmitz, Lars ^a   Georges, Lea ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANCIENT DNA; EGLN1 PROTEIN, HUMAN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYPOXIA INDUCIBLE FACTOR PROLINE DIOXYGENASE; NOS3 PROTEIN, HUMAN;

ACCLIMATIZATION; ARCHEOLOGY; GENETIC DRIFT; GENETIC SELECTION; GENETICS; GENOTYPE; HUMAN; HYPOXIA; MOLECULAR EVOLUTION; PERU;

ACCLIMATIZATION; ARCHAEOLOGY; DNA, ANCIENT; EVOLUTION, MOLECULAR; GENETIC DRIFT; GENOTYPE; HUMANS; HYPOXIA; HYPOXIA-INDUCIBLE FACTOR-PROLINE DIOXYGENASES; NITRIC OXIDE SYNTHASE TYPE III; PERU; SELECTION, GENETIC;

EID: 84961730126     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep23485     Document Type: Article

References (70)

1. Aldenfelder, M. S. In Handb. South Am. Archaeol. (Silverman, H. & Isbell, W. H.) 131-143 (Springer, 2008).
2. Beall, C. M. In High Alt. Hum. Adapt. to Hypoxia (Swenson, E. R. & Baertsch, P.) 357-378 (Springer, 2014).
3. Rademaker, K. et al. Paleoindian settlement of the high-altitude Peruvian Andes. Science 346, 466-469 (2014).
4. Wang, P., Ha, A. Y. N., Kidd, K. K., Koehle, M. S. & Rupert, J. L. A variant of the endothelial nitric oxide synthase gene (NOS3) associated with AMS susceptibility is less common in the Quechua, a high altitude Native population. High Alt. Med. Biol. 11, 27-30 (2010).
5. Moore, L. G. Human genetic adaptation to high altitude. High Alt. Med. Biol. 2, 257-79 (2001).
6. Beall, C. M. Adaptation to High Altitude: Phenotypes and Genotypes. Annu. Rev. Anthropol. 43, 251-272 (2014).
7. Beall, C. M. et al. Hemoglobin concentration of high-altitude Tibetans and Bolivian Aymara. Am. J. Phys. Anthropol. 106, 385-400 (1998).
8. Zhou, D. et al. Whole-genome sequencing uncovers the genetic basis of chronic mountain sickness in Andean highlanders. Am. J. Hum. Genet. 93, 452-62 (2013).
9. Rupert, J. L. & Hochachka, P. W. Genetic approaches to understanding human adaptation to altitude in the Andes. J. Exp. Biol. 204, 3151-3160 (2001).
10. Beall, C. M. Detecting natural selection in high-altitude human populations. Respir. Physiol Neurobiol. 158, 161-171 (2007).
11. Bigham, A. W. et al. Angiotensin-converting enzyme genotype and arterial oxygen saturation at high altitude in Peruvian Quechua. High Alt. Med. Biol. 9, 167-78 (2008).
12. Eichstaedt, C. A. et al. The Andean adaptive toolkit to counteract high altitude maladaptation: genome-wide and phenotypic analysis of the Collas. Plos One 9, e93314 (2014).
13. Sabeti, P. C. et al. Genome-wide detection and characterization of positive selection in human populations. Nature 449, 913-8 (2007).
14. Hancock, A. M. & Rienzo, A. Di. Detecting the Genetic Signature of Natural Selection in Human Populations: Models, Methods, and Data. Annu. Rev. Anthropol. 37, 197-217 (2008).
15. Wilde, S. et al. Direct evidence for positive selection of skin, hair, and eye pigmentation in Europeans during the last 5,000 y. Proc. Natl. Acad. Sci. USA 111, 4832-7 (2014).
16. O'Fallon, B. D. & Fehren-Schmitz, L. Native Americans experienced a strong population bottleneck coincident with European contact. Proc. Natl. Acad. Sci. USA 108, 20444-20448 (2011).
17. Reich, D. et al. Reconstructing Native American population history. Nature 488, 370-374 (2012).
18. Sverrisdóttir, O. Ó. et al. Direct estimates of natural selection in Iberia indicate calcium absorption was not the only driver of lactase persistence in Europe. Mol. Biol. Evol. 31, 975-83 (2014).
19. Chatterjee, A., Black, S. M. & Catravas, J. D. Endothelial nitric oxide (NO) and its pathophysiologic regulation. Vascul. Pharmacol. 49, 134-40 (2008).
20. Schoene, R. B. Unraveling the mechanism of high altitude pulmonary edema. High Alt. Med. Biol. 5, 125-35 (2004).
21. Niu, W. & Qi, Y. An updated meta-analysis of endothelial nitric oxide synthase gene: three well-characterized polymorphisms with hypertension. Plos One 6, e24266 (2011).
22. Lykke, J. A. et al. Vascular associated gene variants in patients with preeclampsia: results from the Danish National Birth Cohort. Acta Obstet. Gynecol. Scand. 91, 1053-60 (2012).
23. Bigham, A. et al. Identifying signatures of natural selection in Tibetan and Andean populations using dense genome scan data. Plos Genet. 6, e1001116 (2010).
24. Ronen, R., Zhou, D., Bafna, V. & Haddad, G. G. The genetic basis of chronic mountain sickness. Physiol. 29, 403-412 (2014).
25. Altshuler, D. M. et al. An integrated map of genetic variation from 1,092 human genomes. Nature 491, 56-65 (2012).
26. Bigham, A. W. et al. Andean and Tibetan patterns of adaptation to high altitude. Am. J. Hum. Biol. 25, 190-7 (2013).
27. Fehren-Schmitz, L., Reindel, M., Tomasto-Cagigao, E., Hummel, S. & Herrmann, B. Pre-Columbian Population Dynamics in Coastal Southern Peru: A Diachronic Investigation of mtDNA Patterns in the Palpa Region by Ancient DNA Analysis. Am. J. Phys. Anthropol. 141, 208-221 (2010).
28. Fehren-Schmitz, L. et al. Climate change underlies global demographic, genetic, and cultural transitions in pre-Columbian southern Peru. Proc. Natl. Acad. Sci. USA 111, 9443-9448 (2014).
29. Fehren-Schmitz, L. et al. A Re-Appraisal of the Early Andean Human Remains from Lauricocha in Peru. Plos One 10, e0127141 (2015).
30. Georges, L., Seidenberg, V., Hummel, S. & Fehren-Schmitz, L. Molecular characterization of ABO blood group frequencies in pre-Columbian Peruvian highlanders. Am. J. Phys. Anthropol. 149, 242-249 (2012).
31. Fehren-Schmitz, L., Llamas, B., Tomasto-Cagigao, E. & Haak, W. El ADN antiguo y la historia del poblamiento temprano del oeste de sudamerica: Lo que hemos aprendido y hacia donde vamos. Bol. Arqueol. PUCP 15, 17-42 (2012).
32. Fehren-Schmitz, L. et al. Diachronic investigations of mitochondrial and y-chromosomal genetic markers in pre-columbian andean highlanders from South peru. Ann. Hum. Genet. 75, 266-283 (2011).
33. Seidenberg, V. et al. A new miniSTR heptaplex system for genetic fingerprinting of ancient DNA from archaeological human bone. J. Archaeol. Sci. 39, 3224-3229 (2012).
34. Malmstrom, H. et al. More on contamination: The use of asymmetric molecular behaviour to identify authentic ancient human DNA. Mol. Biol. Evol. 24, 998-1004 (2007).
35. Sandoval-Castellanos, E. Testing temporal changes in allele frequencies: a simulation approach. Genet. Res. (Camb). 92, 309-20 (2010).
36. Waples, R. S. Temporal Variation in Allele Frequencies: Testing the Right Hypothesis tle. Evolution (N. Y). 43, 1236-1251 (1989).
37. Piccoli, J. C. E. et al. Association between 894G > T endothelial nitric oxide synthase gene polymorphisms and metabolic syndrome. Arq. Bras. Endocrinol. Metabol. 52, 1367-1373 (2008).
38. Carnese, F. R. et al. Paleogenetical study of pre-Columbian samples from Pampa Grande (Salta, Argentina). Am. J. Phys. Anthropol. 141, 452-462 (2010).
39. Moore, L. G. et al. Maternal adaptation to high-altitude pregnancy: an experiment of nature-a review. Placenta 25 Suppl A, S60-S71 (2004).
40. Fehren-Schmitz, L., Reindel, M., Tomasto-Cagigao, E., Hummel, S. & Herrmann, B. Pre-Columbian population dynamics in coastal southern Peru: A diachronic investigation of mtDNA patterns in the Palpa region by ancient DNA analysis. Am. J. Phys. Anthropol. 141, 208-221 (2010).
41. Kemp, B. M., Tung, T. A. & Summar, M. L. Genetic continuity after the collapse of the Wari empire: Mitochondrial DNA profiles from Wari and post-Wari populations in the ancient Andes. Am. J. Phys. Anthropol. 140, 80-91 (2009).
42. Bisso-Machado, R., Bortolini, M. C. & Salzano, F. M. Uniparental genetic markers in South Amerindians. Genet. Mol. Biol. 35, 365-87 (2012).
43. Wang, S. et al. Genetic Variation and Population Structure in Native Americans. Plos. Genet. 3, e185 (2007).
44. Lewis, C. M. et al. Mitochondrial DNA and the Peopling of South America. Hum. Biol. 79, 159-178 (2007).
45. Dufour, D. L. & Piperata, B. A. Rural-to-urban migration in Latin America: an update and thoughts on the model. Am. J. Hum. Biol. 16, 395-404 (2004).
46. Osier, M. V. et al. ALFRED: An allele frequency database for anthropology. Am. J. Phys. Anthropol. 119, 77-83 (2002).
47. Tamm, E. et al. Beringian standstill and spread of Native American founders. Plos. One. 2, e829 (2007).
48. Julian, C. G. et al. High-altitude ancestry protects against hypoxia-associated reductions in fetal growth. Arch. Dis. Child Fetal Neonatal Ed 92, 372-377 (2007).
49. Laland, K. N., Odling-Smee, J. & Feldman, M. W. Cultural niche construction and human evolution. J. Evol. Biol. 14, 22-33 (2001).
50. Tishkoff, S. A. et al. Convergent adaptation of human lactase persistence in Africa and Europe. Nat. Genet. 39, 31-40 (2007).
51. Tishkoff, S. A. et al. Haplotype diversity and linkage disequilibrium at human G6PD: recent origin of alleles that confer malarial resistance. Science 293, 455-62 (2001).
52. Jeong, C. et al. Admixture facilitates genetic adaptations to high altitude in Tibet. Nat. Commun. 5, 3281 (2014).
53. Xiang, K. et al. Identification of a Tibetan-specific mutation in the hypoxic gene EGLN1 and its contribution to high-altitude adaptation. Mol. Biol. Evol. 30, 1889-98 (2013).
54. Coutinho, A. et al. AmericaPlex26: A snapshot multiplex system for genotyping the main human mitochondrial founder lineages of the Americas. Plos One 9, e93292 (2014).
55. Doi, Y. et al. A new method for ABO genotyping using a multiplex single-base primer extension reaction and its application to forensic casework samples. Leg. Med. (Tokyo) 6, 213-223 (2004).
56. Peakall, R. & Smouse, P. E. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28, 2537-9 (2012).
57. Livi-Bacci, M. The depopulation of Hispanic America after the conquest. Popul. Dev. Rev. 32, 199-232 (2006).
58. Lewontin, R. C. The Interaction of Selection and Linkage. I. General Considerations; Heterotic Models. Genetics 49, 49-67 (1964).
59. Slatkin, M. Linkage disequilibrium in growing and stable populations. Genetics 137, 331-336 (1994).
60. Excoffier, L. & Lischer, H. E. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 10, 564-567 (2010).
61. Machiela, M. J. & Chanock, S. J. LDlink: A web-based application for exploring population-specific haplotype structure and linking correlated alleles of possible functional variants. Bioinformatics 31, 3555-3557 (2014).
62. Maynard Smith, J. Evolutionary Genetics (Oxford University Press, 1998).
63. Voight, B. F. et al. Interrogating multiple aspects of variation in a full resequencing data set to infer human population size changes. Proc. Natl. Acad. Sci. USA 102, 18508-13 (2005).
64. Fehren-Schmitz, L. et al. A re-appraisal of the early Andean human remains from Lauricocha in Peru. Plos One 10, e0127141 (2015).
65. Kimura, M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111-120 (1980).
66. Ho, S. Y. & Endicott, P. The crucial role of calibration in molecular date estimates for the peopling of the Americas. Am. J. Hum. Genet. 83, 142-146 (2008).
67. Slatkin, M. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139, 457-462 (1995).
68. Bigham, A. W. et al. Identifying positive selection candidate loci for high-altitude adaptation in Andean populations. Hum. Genomics 4, 79-90 (2009).
69. Beall, C. M. et al. Pulmonary nitric oxide in mountain dwellers. Nature 414, 411-2 (2001).
70. Wang, X. L. et al. Genotype dependent and cigarette specific effects on endothelial nitric oxide synthase gene expression and enzyme activity. FEBS Lett. 471, 45-50 (2000).